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Parasites of South African wildlife. XIX. The prevalence of helminths in some common antelopes, warthogs and a bushpig in the Limpopo province, South Africa

Authors: Little work has been conducted on the helminth parasites of artiodactylids in the northern 1 Ilana C. van Wyk and western parts of the Limpopo province, which is considerably drier than the rest of the Joop Boomker1 province. The aim of this study was to determine the kinds and numbers of helminth that Affiliations: occur in different wildlife hosts in the area as well as whether any zoonotic helminths were 1Department of Veterinary present. Ten impalas (Aepyceros melampus), eight kudus (Tragelaphus strepsiceros), four blue Tropical Diseases, University wildebeest (Connochaetes taurinus), two black wildebeest (Connochaetes gnou), three gemsbok of Pretoria, South Africa (Oryx gazella), one nyala (Tragelaphus angasii), one bushbuck (Tragelaphus scriptus), one Correspondence to: waterbuck (Kobus ellipsiprymnus), six warthogs (Phacochoerus aethiopicus) and a single bushpig Ilana van Wyk (Potamochoerus porcus) were sampled from various localities in the semi-arid northern and western areas of the Limpopo province. Email: [email protected] New host–parasite associations included Trichostrongylus deflexus from blue wildebeest, Postal address: Agriostomum gorgonis from black wildebeest, Stilesia globipunctata from the waterbuck and Private bag X04, Fasciola hepatica in a kudu. The mean helminth burden, including extra-gastrointestinal Onderstepoort 0110, South Africa helminths, was 592 in impalas, 407 in kudus and blue wildebeest, 588 in black wildebeest, 184 in gemsbok, and 2150 in the waterbuck. Excluding Probstmayria vivipara, the mean helminth Dates: burden in warthogs was 2228 and the total nematode burden in the bushpig was 80. The Received: 20 Nov. 2010 total burdens and species richness of the helminths in this study were consistently low when Accepted: 29 Aug. 2011 Published: 11 Nov. 2011 compared with similar studies on the same species in areas with higher rainfall. This has practical implications when animals are translocated to areas with higher rainfall and higher How to cite this article: prevalence of helminths. Van Wyk, I.C. & Boomker, J., 2011, ‘Parasites of South African wildlife. XIX. The prevalence of helminths in Introduction some common antelopes, Game ranching constitutes a significant part of the land use practices in the Limpopo province, warthogs and a bushpig in the Limpopo province, South Africa. Parasites play an important role in regulating host populations in a natural South Africa’, Onderstepoort environment; therefore, knowledge about the helminth infections of wildife in an area is essential. Journal of Veterinary Farming with game creates an unnatural system and disrupts the balance between parasite and Research 78(1), Art. #308, host. In this stressful environment animals become diseased or can even die from parasite loads 11 pages. http://dx.doi. org/10.4102/ojvr.v78i1.308 that they would have survived under natural conditions. Trophy hunting and the production of venison are increasing in the province and condemnation of carcasses due to macroscopic pathology caused by parasites can lead to financial losses.

Little work has been conducted on the helminth parasites of artiodactylids in the northern and western parts of the province. The aims of this study were to determine the species and numbers of helminth that occur in different wildlife hosts in the area, and to determine whether any zoonotic helminths were present. To this end, a total of 37 animals from various localities in the Limpopo province were examined and their parasites identified and counted. Materials and methods Materials The animal species, number of collections and the collection dates and localities (with their global positioning system coordinates) are summarised in Table 1.

© 2011. The Authors. Survey areas Licensee: AOSIS The survey was performed in the northern parts of the Limpopo province near the Soutpansberg OpenJournals. This work and the town Musina, which lies on the Limpopo River, and the western parts near the town is licensed under the Creative Commons Lephalale. The vegetation in the Soutpansberg region is Mixed Bushveld with sections falling Attribution License. within the mist belt on the escarpment. The Musina area is semi-arid and the vegetation type

http://www.ojvr.org doi:10.4102/ojvr.v78i1.308 Page 2 of 11 Original Research varies between Thornveld and Mopani veld (Acocks 1988). In addition to the warthogs (Phacochoerus aethiopicus) that The rainfall recorded between July 2006 and June 2007 for had been culled, the carcasses of several warthogs from a the Soutpansberg area and Musina was 300 mm and 500 mm, meat processing plant were examined for Trichinella spp. As respectively (South African Weather Service 2007). Rainfall only the eviscerated carcasses were available, only samples is strictly confined to the summer. The climate is hot during from the diaphragms and the intercostal muscles could be summer and cool during winter, with occasional frost. collected for examination.

The western parts of the province are semi-arid and the Collection and preservation of parasites vegetation type varies between Sweet Bushveld and Mixed The carcasses of the culled animals were first inspected Bushveld (Acocks 1988). Rainfall from July 2006 to July 2007 visually for the presence of Taenia or Echinococcus in the Lephalale area was 178 mm (South African Weather metacestodes on the cut surfaces and those of the pericardium, Service 2007). The summers are hot and the winters cool. heart, diaphragm and liver. When permitted, the tongue was freed and examined visually and palpated. Only single Study animals metacestodes were encountered and collected, which were subsequently preserved in 70% alcohol. With the exception of one gemsbok (Oryx gazella) and the nyala (Tragelaphus angasii), the study material was obtained Carcasses that were destined for export were not skinned from animals that had been culled or hunted during the until they reached the abattoir. No incisions were made into hunting season (May–September) of 2006 and 2007. A few the muscles, except for the masseter and the diaphragm. organ samples from one of the gemsbok and the carcass of The heads and capes of animals hunted for trophies were the nyala were submitted to the Louis Trichardt Veterinary preserved; therefore, no incisions of the masseter muscles or Laboratory for post-mortem examination. tongues could be made.

TABLE 1: The collection data for the various animals examined. Species n Date Locality Farm GPS coordinates Impala 3 Jun. 2006 Musina Musina Research Station 22°40.645S 29°48.895E 1 Jul. 2007 1 Jun. 2006 Musina Kerneels Young Trust 22°40.645S 29°48.895E 2 Jun. 2006 Lephalale Bushman’s Safaris 23°10.086S 28°05.189E 3 Aug. 2007 Soutpansberg Nwanedi Nature Reserve 22°56.129S 29°55.003E Kudu 3 May 2007 Soutpansberg Langgedachte 23°19.985S 29°48.075E 2 Jul. 2007 Musina Musina Research Station 22°40.645S 29°48.895E 1 Jun. 2006 Musina Kerneels Young Trust 22°40.645S 29°48.895E 1 Jul. 2007 Lephalale Bushman’s Safaris 23°10.086S 28°05.189E 1 Aug. 2007 Soutpansberg Nwanedi Nature Reserve 22°56.129S 29°55.003E Bushbuck 1 Aug. 2007 Soutpansberg Last Post 23°17.557S 29°54.593E Nyala 1 Sep. 2007 Soutpansberg Uitvlught 23°02.903S 29°46.035E Blue wildebeest 3 Aug. 2007 Soutpansberg Langgedachte 23°19.985S 29°48.075E 1 Jul. 2006 Lephalale Bushman’s Safaris 23°10.086S 28°05.189E Black wildebeest 2 Jul. 2007 Lephalale Bushman’s Safaris 23°10.086S 28°05.189E Gemsbok 2 Jul. 2007 Musina Musina Research Station 22°40.645S 29°48.895E 1 Jun. 2006 Musina Kerneels Young Trust 22°40.645S 29°48.895E Waterbuck 1 Jul. 2007 Soutpansberg Last Post 23°17.557S 29°54.593E Warthog 2 Aug. 2006 Lephalale Bushman’s Safaris 23°10.086S 28°05.189E 2 Aug. 2007 1 Jun. 2006 Musina Kerneels Young Trust 22°40.645S 29°48.895E 1 Jun. 2007 Musina Alldays 22°45.639S 29°48.523E Bushpig 1 Oct. 2007 Soutpansberg Soekmekaar 23°17.557S 29°54.593E GPS, global positioning system; n, sample size.

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The intestinal helminths as well as those in the heart, lungs Data analysis and liver of the antelopes were collected as described by Sampling was not truly random and depended on Boomker, Horak and De Vos (1989) but digests of abomasal circumstances to some extent. Therefore, the significance of and intestinal mucosae were not performed. Depending the results could not be compared statistically. However, on the volume of ingesta of the different parts of the descriptive statistics were used as applicable. gastrointestinal tract, aliquots of a quarter, a tenth or a 25th were made and examined. The entire abomasal content of the bushbuck (Tragelaphus scriptus) was examined. Ethical considerations The samples in this study were opportunistically collected The helminths of warthogs and the bushpig (Potamochoerus from animals that had been either hunted or culled for porcus) were recovered as described by Boomker et al. reasons other than this study. (1991a). In addition, muscle samples from the diaphragm and intercostal and masseter muscles were crushed (between glass slides) and examined under a stereoscopic microscope Results and discussion for the presence of Trichinella spp. Animals Impalas Parasite counts and identification Twelve helminth species, ten nematodes and two cestodes Aliquots of ingesta and organ washings were fixed and were recovered from impalas (Aepyceros melampus) in this preserved in 70% ethyl alcohol. These were transported to the study. The helminth burdens are presented in Table 2. laboratory, where they were examined under a stereoscopic microscope and all helminths were removed. The nematodes Cooperia hungi was most prevalent, followed by were cleared in lactophenol, identified under a standard Impalaia tuberculata, Oesophagostomum columbianum and microscope and counted. Male nematodes were identified to Trichostrongylus deflexus. Haemonchus krugeri had the highest species level, whereas female nematodes, especially where mean intensity (375 worms), followed by C. hungi (280 two or more related species occurred in a single host, were worms) and I. tuberculata (140 worms). identified to the generic level only. Fourth-stage larvae were identified only to the generic level. Impala and their parasites have been studied by several authors and some significant contributions have been made Live adult cestodes were relaxed in water in Petri dishes. by Anderson (1992), Heinichen (1973), Horak (1978, 1980, Once all movement had ceased they were fixed in %5 formalin 1981) and Mönnig (1933) in South Africa and Gallivan et al. for 24 h and further preserved in 70% ethyl alcohol. Scoleces (1989) in Swaziland. Because of their feeding ecology, impala were dissected out of the metacestodes and mounted en face are exposed to the helminths of both browsers and grazers. in Berlese’s fluid under slight pressure from a cover slip. Impala also share pastures with domestic livestock on many Adult cestodes were stained in carmalum or Mayer’s acid game ranches in South Africa and considerable overlap haemalum, cleared in xylene and mounted on glass slides in between the helminth fauna of sheep, cattle and impalas Canada balsam (Gibbons, Jones & Kahlil 1996). occurs (Horak 1978).

TABLE 2: Total helminth burdens of examined impala. Species Lephalale area Musina area Soutpansberg area Mean Prevalence (n = 10) (%) BI1† BI2† BI3† MI1† MI2† MI3† YI1† NwI1† NwI2† NwI3† Cooperia fuelleborni - - - - - 75 - - - - 7 10 Cooperia hungi 150 100 - 75 500 25 450 475 475 275 253 90 Cooperia L4 ------200 - - - 20 10 Cooperioides hamiltoni 200 75 ------28 20 Cooperioides hepaticae ------10 - 20 3 20 Haemonchus krugeri 350 - 400 ------75 20 Haemonchus L4 25 - - 25 ------5 20 Impalaia tuberculata - 75 - - - - 225 325 25 50 70 50 Impalaia L4 225 ------23 10 Longistrongylus sabie - - - - - 50 - - - - 5 10 Oesophagostomum columbianum 125 25 250 - 25 - - 25 - - 40 50 Oesophagostomum L4 ------225 - - 23 10 Trichostrongylus colubriformis ------150 25 18 20 Trichostrongylus deflexus 25 25 - 50 - 75 - - - - 18 40 Moniezia expansa - - - - 5 - - - - - 1 10 Stilesia hepatica ------7 1 10 Total burden 1100 300 650 25 550 250 875 1100 650 377 588 - L4, fourth-stage larvae. †, Individual animal number.

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Cooperia hungi is considered a definitive parasite of impalas The lowest burden was six worms, comprising the two and the other nine nematode species all occurred in five or species Elaeophora sagitta and Fasciola hepatica, which both use fewer animals, which classifies them as either occasional or intermediate hosts. The mean helminth burden, including E. accidental parasites (Horak 1980). sagitta and F. hepatica, was 407 worms.

In Horak’s (1978) study on impala at Nylsvley, more than Haemonchus contortus was the most prevalent worm and was 90% of the worms were retarded in the fourth stage at recovered from six of the eight kudus, followed by E. sagitta different times of the year. As digests were not carried out recovered from three kudus. in this study, the recovery rate of larval stages was low, Haemonchus vegliai which may account for the low total helminth counts. The According to the criteria of Horak (1980), , Cooperia neitzi, Cooperia acutispiculum, E. sagitta and T. deflexus harsh environment in the northern and western parts of the are definitive parasites of kudus in the Kruger National Park Limpopo province would necessitate helminth parasites (Boomker et al. 1989) and in the Eastern Cape (Boomker, Horak to employ strategies to protect the vulnerable, free-living & Knight 1991b). The amphistomes, Schistosoma mattheei, larval stages, not only during winter when temperatures and Moniezia benedeni, Taenia larvae, I. tuberculata, Agriostomum rainfall are low, but also during summer, when temperatures gorgonis and Strongyloides papillosus are considered occasional are high and rainfall often low. Owing to the higher rainfall parasites in kudu (Boomker et al. 1991b). and milder climate at Nylsvley it is doubtful whether the same levels of larval retardation exist for worms in the Kudus are known to harbour parasites from other species current study area. of antelopes. Boomker et al. (1991b) found that kudus in the Addo Elephant National Park harboured Nematodirus The relatively few helminth species recovered could also be helvetianus and Dictyocaulus spp., thought to originate from due to a smaller diversity of antelope species in the sampling cattle in the area. The H. contortus recovered in the current areas. Where a large number of antelope species are present, study probably originated from goats. Cooperioides hamiltoni, cross-transmission can take place more readily (Boomker, a parasite described from impalas, was recovered from Anthonissen & Horak 1988), which increases the diversity of kudus in this study and is considered an occasional parasite parasite species. of kudus (Boomker et al. 1988).

Except for one kudu from the Soutpansberg area, the Although two impalas from Nwanedi in the Soutpansberg helminth burdens were relatively low but the range was had eosinophilic granulomata in the lungs, no parasites similar for that of kudu sampled in the Etosha Game Reserve were recovered from these lesions. The most common gross (Boomker et al. 1988) and the Eastern Cape (Boomker et al. lesions associated with the lungworm Pneumostrongylus 1991b). This is in contrast to kudus sampled in the Kruger calcaratus in impalas in Swaziland were firm nodules along National Park (Boomker et al. 1989), which showed much the lateral borders of the caudal lung lobes (Gallivan et al. higher burdens. The kudus were mainly from the southern 1989). Those authors recorded an 85% prevalence of this region of the park, which has an annual rainfall of 600 mm – nematode in impalas in Mlawula Nature Reserve, Swaziland. 700 mm. The dry climate of the localities in the present study Pneumostrongylus calcaratus has been found to be prevalent area is more similar to that in Etosha and the Eastern Cape in the eastern Transvaal Lowveld (now Limpopo and and is too harsh for the survival of the free-living infective Mpumalanga) as indicated by Ortlepp (1962) and Young stages of helminths (Boomker et al. 1989). and Wagener (1968), and in the northern part of KwaZulu- Natal (Anderson 1992). Young and Wagener (1968) found a Of the helminths considered definitive parasites of kudu in high prevalence in impala in the southern Kruger National the Kruger National Park (Boomker et al. 1989) only C. neitzi Park, whereas Horak (1978, 1980) did not recover lungworms and E. sagitta were recovered from the kudus in this study. from impalas at Nylsvley Nature Reserve or from Pafuri in However, C. neitzi was recovered only in one kudu and in the northern Kruger National Park. Horak (1981) ascribed small numbers. Elaeophora sagitta was recovered from three this difference in prevalence to climate. He suggested that kudus from two of the localities in this study and also not Pneumostrongylus is restricted to warm, moist regions, in significant numbers. Their presence is an indication of the where the mollusk intermediate host (Urocyclus [Elisolimax] abundance of their intermediate host (Boomker 2007). flavescens) occurs. Because kudus are browsers and roam considerably they are subject to reinfection with their own parasites only to a Kudus limited extent (Boomker, Horak & De Vos 1986). However, Five nematode species and one trematode were recovered animals that roam are more likely to become infected with from kudus (Tragelaphus strepsiceros) in this study. The total accidental parasites (Horak 1980). Agriostomum gorgonis and worm burdens are summarised in Table 3. Oesophagostomum spp. are considered accidental parasites as they occurred only in one kudu each and in low numbers. The kudu with the highest burden had 2690 worms, of which 2425 were Haemonchus contortus. Excluding this kudu, the Bushbuck mean burden for the remaining seven kudus was 81 worms. No parasites were recovered from the single animal recovered This is a classical example of overdispersion of the parasites. in this survey. This may be a result of underdispersion or

http://www.ojvr.org doi:10.4102/ojvr.v78i1.308 Page 5 of 11 Original Research the low stocking densities of antelopes on the farm of origin, The seasonal patterns of several parasites of wildebeest which, in turn, will also limit the exposure of animals to from the Kruger National Park have been attributed to a infection or cross-infection with helminths. combination of climatic factors and migratory patterns of the wildebeest in the park (Horak et al. 1983b). On small game Nyala farms animals generally have limited migration patterns The carcass of the nyala bull was submitted to the Louis and therefore the risk of becoming reinfected from the Trichardt Veterinary Laboratory for a post-mortem contaminated pastures increase. examination in October 2007. Clostridium novyi was diagnosed as the cause of death. The animal was in poor condition and Black wildebeest died during the rutting season. It was expected that the One of the two black wildebeest (Connochaetes gnou) sampled animal would have harboured some parasites under these harboured 100 H. bedfordi only. The other presented with a conditions, yet none was recovered. The nyala originated total of 1075 worms, comprising 50 A. gorgonis, 875 H. bedfordi from a farm where cattle and antelopes shared the same and 150 O. columbianum. pasture. Deworming of cattle could be a possible reason for the absence of helminths as the parasite contamination on the The helminths of black wildebeest have received little pasture would be reduced. Also, the nyala died at the end of the dry season, before the first spring rains, when larvae were attention (Boomker et al. 2000). Wildebeest appear to be fairly still in hypobiosis or absent from the pasture. resistant to parasitic infections, as animals from the Golden Gate Highlands National Park and Rietvlei Nature Reserve Blue wildebeest harboured relatively low burdens of only a small number of Five nematode species were recovered from blue wildebeest helminth species when compared with blue wildebeest from (Connochaetus taurinus) in this study and their burdens are the Kruger National Park (Horak et al. 1983b). In an earlier summarised in Table 4. study, Boomker et al. (2000) found that a black wildebeest from the Mountain Zebra National Park harboured a The highest total burden in an animal was 550 worms. The single Taenia sp. larva, 26 Haemonchus spp. females and one mean helminth burden of the four blue wildebeest was 407 Haemonchus spp. larva. Neither of two black wildebeest worms. The species with the highest intensity was H. contortus from the Karoo National Park sampled during that study (500 per individual), followed by Haemonchus bedfordi (375 harboured any worms (Boomker et al. 2000). per individual). This parasite appears to be common in blue wildebeest and has been recovered from animals from Gemsbok the Kruger National Park (Horak, De Vos & Brown 1983b) as well as from the Kalahari Gemsbok National Park (now Two nematode species and the larval stages of two cestode Kgalagadi Transfrontier Park) (Boomker et al. 1986). species were recovered from the gemsbok sampled in the present study. One of the two gemsbok from Musina had Cooperia connochaeti was recovered from three of the four blue 350 C. hungi, one Setaria hornbyi and seven Taenia hydatigena wildebeest in this study. It is considered a definitive parasite larvae, whilst the other had no nematodes and only six T. for this species. hydatigena and three Taenia hyaenae larvae. The gemsbok from

TABLE 3: Total helminth burdens of examined kudu. Species Soutpansberg area Lephalale Musina area Mean Prevalence (n = 8) (%) VK1† VK2† VK3† NwK1† BK1† YK1† MK1† MK2† Agriostomum gorgonis - - 25 - - - - - 3 12.5 Cooperia neitzi - - 240 - - - - - 30 12.5 Elaeophora sagitta - - - 4 - - 85 1 12 37.5 Haemonchus contortus 50 275 2425 - 50 - 50 25 359 75.0 Oesophagostomum L4 - - - - - 25 - - 3 12.5 Fasciola hepatica - - - 2 - - - - 0 12.5 Total burden 50 275 2690 6 50 25 135 26 407 - L4, fourth-stage larvae. †, Individual animal number.

TABLE 4: Total helminth burdens of examined blue wildebeest. Species Soutpansberg area Lephalale Mean Prevalence (n = 4) (%) VWB1† VWB2† VWB3† BWB1† Cooperia connochaeti 75 175 - 125 94 75 Haemonchus bedfordi - - - 375 94 25 Haemonchus contortus 100 175 500 - 194 75 Oesophagostomum columbianum - - - 50 12 25 Trichostrongylus deflexus 25 - 25 - 12 50 Moniezia benedeni - - fragments - - 25 Total burden 200 350 525 550 407 - †, Individual animal number.

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Kerneels Young Trust harboured three calcified Setaria spp. Two nematode genera occurred in all the warthogs, namely and two T. hydatigena larvae. Oesophagostomum mwanzae and Probstmayria vivipara. Murshidia hamata was recovered from four of the six warthogs The larval stages of T. hydatigena were found attached and Oesophagostomum mocambiquei from three. Murshidia to the mesenterium and liver of all three gemsbok. The T. pugnicaudata was recovered from only two warthogs. hyaenae larvae occurred in the triceps and heart muscles. The Hydatid cysts of Echinococcus granulosus were recovered metacestodes were identified according to the number and from the lungs of one of the warthogs. size of their rostellar hooks (Verster 1969).

The helminth with the highest intensity was P. vivipara, with Although gemsbok are relatively common in the Limpopo province, they are historically not endemic to this region. The burdens ranging between 276 000 and 825 000 per host. The translocation of antelopes to climatic or vegetation regions helminth with the second highest intensity was O. mwanzae, where they did not occur historically can be hazardous to with a total burden of 3700 recovered from one warthog. their health (Boomker et al. 2000). Earlier studies found the total helminth burden of gemsbok from the West Coast The highest total helminth burden that included P. vivipara, National Park, where the antelopes do not naturally occur, was 825 940 including for warthog BWh1. However, warthog to be 28 681 (Boomker et al. 2000), compared with 5877 for BWh3 had the highest helminth burden (5920) that excluded gemsbok from the Kalahari Gemsbok National Park (now P. vivipara. Kgalagadi Trasfrontier Park) (Boomker et al. 1986). The high burden for gemsbok in the West Coast National Park No Trichinella were found in any of the carcasses. is attributed to the climatic conditions in the area, as the climate appeared to favour parasites but caused stress in the Four of the warthogs originated from Bushman’s Safaris, two gemsbok (Boomker et al. 2000). In the Limpopo province the of which were examined in August 2006 and two in August climate is rather similar to that of the Kalahari, which may 2007. The two warthogs from the 2006 sample harboured be the reason for the small numbers of helminths recovered Murshidia spp. but no O. mocambiquei, but the converse was from gemsbok in the present study. true for the warthogs examined in 2007. The two warthogs sampled in 2006 also had lower total helminth burdens Waterbuck (excluding P. vivipara), namely 162 and 702, respectively. Five helminth species were recovered from the waterbuck The warthogs sampled in 2007 had total burdens (excluding (Kobus ellipsiprymnus), namely Cooperia curticei, Trichuris spp., P. vivipara) of 5920 and 4810, respectively. It is possible that O. columbianum, Avitellina spp. and Stilesia globipunctata. The although Lephalale had below-average rainfall during the helminth with the highest intensity was C. curticei (2075), followed by Trichuris spp. (50) and O. columbianum (25). This 2006/2007 season, rain during the dry season in 2007 could is approximately half of what was recovered from a single have affected the abundance of parasites in the region. waterbuck from Pretoriuskop in the Kruger National Park, which harboured 4082 helminths (Boomker et al. 1986) and The helminths of warthogs in southern Africa have been included H. bedfordi (813), Cooperia fuelleborni (1524), C. hungi described by several authors, including Boomker et al. (363), Cooperia yoshidai (1088), I. tuberculata (225) and O. (1991a), Horak et al. (1983a, 1988) and Ortlepp (1964). The columbianum (25) (Boomker et al. 1986). helminth parasites of warthogs as listed by Round (1968) include parasites from across Africa. However, many Warthogs helminths occur only in certain regions as is evident from Ten helminth species were recovered from the warthogs in the work of Ortlepp (1964), Horak et al. (1983a, 1988) and this study. The total burdens of each parasite are presented Boomker et al. (1991a). in Table 5.

TABLE 5: Total helminth burdens of examined warthogs. Species Musina Lephalale Mean Prevalence (n = 6) (%) YWh1† AWh1† BWh1† BWh2† BWh3† BWh4† Cooperia hungi 4 - - - - - 0 17 Impalaia tuberculata - - - 12 - - 2 17 Murshidia hamata 50 90 90 250 - - 80 67 Murshidia pugnicaudata 35 - - 80 - - 20 33 Oesophagostomum mocambiquei - 380 - - 2300 1100 1064 50 Oesophagostomum mwanzae 1075 130 850 350 3600 3700 1185 100 Probstmayria vivipara 276 000 380 000 825 000 407 000 648 000 470 000 501 000 100 Physocephalus sexalatus 3 - 27 13 20 9 12 83 Echinococcus sp. cyst - - - - - 1 0 17 Paramonezia phacochoeri - - - 1 - - 0 17 Total helminth burden 277 167 38 600 825 967 407 706 653 920 474 810 50335 - Total burden excluding P. vivipara 1167 600 967 706 5920 4810 2363 - †, Individual animal number.

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Bushpig animals sampled were all adults and thus would have had A total of 80 worms representing two nematode species, an acquired immunity. Also, the animals were all sampled namely Physocephalus sexalatus (10) and Globocephalus versteri before the start of the rainy season and therefore the peak (70), were recovered from the single bushpig. burdens of this parasite might have been missed. The dry climate of the study area will affect the survival of free-living The total worm burden of the bushpig was low compared stages of the parasites. with that of warthogs. Ortlepp (1964) made no note of the burdens of the worms he recovered from bushpigs. Because Elaeophora only one animal was examined, a low burden due to Elaeophora sagitta is a definitive parasite of the tragelaphine underdispersion could not be ruled out. antelopes (Boomker et al. 1988). This worm was recovered only from three kudus (i.e. none were recovered from the Little work has been conducted on the helminth parasites bushbuck or nyala) during the current study. This can be of bushpigs. Ortlepp (1964) examined material from because neither the parasite nor its vector, thought to be a Mozambique and the northern Transvaal (now Limpopo), tabanid fly (Boomkeret al. 1986), is common in the study area. which has been included in the list of helminth parasites of Round (1968). Bushpigs are difficult to sample because of Haemonchus their largely nocturnal activity and their relatively limited Haemonchus contortus was the most prevalent worm in kudus distribution in forested areas. in this study. It was recovered from six kudus from three different localities in the study area. Except for one kudu, the Helminths individual burdens of the worm was small. Agriostomum At Langgedachte, H. contortus was collected from three blue Agriostomum gorgonis was recovered only from one kudu wildebeest and three kudus. At this game farm, domestic and one black wildebeest, and in small numbers from both livestock and game are kept together. Haemonchus contortus animals. It is considered an occasional parasite of kudus in is considered a parasite of domestic animals and the high the Kruger National Park (Boomker et al. 1989). No record prevalence is possibly due to cross-transmission from could be found of the worm in black wildebeest, but it has domestic animals and the high stocking densities on the farm. been listed as a parasite of blue wildebeest (Horak et al. 1983b; Round 1968). The free-living stages of hookworms Impalaia require moist climatic conditions for survival and the low Impalaia tuberculata is a parasite of several antelope species, rainfall in the present study area would have been limiting to in particular impalas and blesbok, (Damaliscus dorcas phillipsi) the survival of the larvae of these parasites. (Boomker 1977; Horak 1978). It was recovered from only one warthog in this study. Warthogs are not considered to Cooperia be definitive hosts of these parasites (Boomker et al. 1991a; Cooperia hungi was recovered from only one warthog in this Horak et al. 1988) and infection was probably accidental. study. It has previously been recovered from warthogs at Hoedspruit in the eastern Transvaal (now eastern part of Murshidia the Limpopo province) (Boomker et al. 1991a). It is primarily Ortlepp (1964) recovered M. hamata from Pilgrim’s Rest and a parasite of impala (Horak 1978) and is considered an Zululand, but M. pugnicaudata only from Pilgrim’s Rest. accidental parasite in warthogs (Boomker et al. 1991a). No Murshidia spp. have been recovered from warthogs in Namibia (Horak et al. 1983a). Both species have been Cooperioides recovered from warthogs from Hoedspruit (Boomker et al. Cooperioides hepaticae is the only extra-intestinal 1991a) and the Kruger National Park (Horak et al. 1988). Only trichostrongyloid of impalas and is considered a common M. hamata has been recovered from warthogs in the north- parasite of impalas in the Kruger National Park (Pletcher western Transvaal (now the Limpopo province) (Boomker et et al. 1988; Young & Wagener 1968). Pletcher et al. (1988) al. 1991a). Between 50 and 250 M. hamata were recovered from suggest that smaller burdens in adult impalas compared four of the warthogs in this study. Murshidia pugnicaudata, with yearlings may be due to acquired partial immunity however, was recovered in small numbers from only two in adults due to previous exposure. Cooperioides hepaticae is animals: one from the Musina area in the north and the other generally considered to be of minor pathological significance from the Lephalale area in the west. Both species therefore unless it is present in large numbers in combination with occur in the north, east and west of the province, but M. other trichostrongyles, or when burdens are associated with pugnicaudata possibly not in the north-west. However, it is poor nutritional conditions (Pletcher et al. 1988). not stated from where the warthogs in the north-western Transvaal originated (Boomker et al. 1991a). It should In the present study, C. hepaticae was recovered from only be noted that M. pugnicaudata was recovered only from two impalas and both had very small burdens. One reason warthogs examined during 2006. It is possible that climatic for the low prevalence and intensity could be that the factors played a role in the prevalence of the parasites.

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Oesophagostomum the waterbuck in the current study. The spicules of the male Oesophagostomum columbianum is a common parasite of many measured 5.8 mm in length and did not end in a bulb or antelope species (Boomker 2007). It was the most prevalent swelling either. It is possible that the specimen collected from helminth in this study and was recovered from four hosts, the waterbuck was T. barbertonensis. namely the waterbuck, blue and black wildebeest, and impalas. In none of these animals did this worm occur in Many Trichuris spp., of which T. globulosa is the most large numbers. The typical lesions in the large intestines widespread, have been reported to occur in antelopes in of sheep due to O. columbianum infestation were not found southern Africa (Ortlepp 1937). Trichuris spp. are of greater in any of the examined animals. Horak (1981) considers O. concern in enclosures and zoos than in open spaces owing to columbianum as a definitive parasite of impala. their monoxenous life cycle and thick-shelled eggs (Boomker 2007). Environmental build-up of the parasite is not likely to Both O. mwanzae and O. mocambiquei have been recovered happen in a free-range system. from warthogs from Hoedspruit (Boomker et al. 1991a), the Kruger National Park (Horak et al. 1988) and Pilgrim’s Avitellina Rest (Ortlepp 1964). Both species were also recovered in Avitellina spp. is common in semi-arid areas (Reinecke 1983) this study from animals that originated from the Musina but was recovered only from the waterbuck. and Lephalale areas. It would appear that these are the only two Oesophagostomum species that occur in warthogs in the Stilesia Limpopo and Mpumalanga provinces. Although O. mwanzae Stilesia globipunctata fragments were recovered from the is the dominant of the two species, both can be considered waterbuck. No previous record of this parasite in waterbuck definitive parasites of warthogs in the area. could be found. Both Stilesia and Avitellina require an invertebrate intermediate host, such as oribatid soil mites. Setaria Adult worms are therefore more likely to be found in animals Setaria spp. are filarid worms and the adults are usually that feed close to the ground (Boomker et al. 1986). found in the abdominal cavity of their hosts. Mosquitoes are the intermediate hosts (Reinecke 1983). The Setaria spp. are In this study Stilesia hepatica was recovered from only one considered non-pathogenic and are usually found only at impala. Gallivan et al. (1996) reported no difference between necropsy. seasons or sexes, but in their study adult animals had larger burdens, possibly indicating that it is an accumulative Trichostrongylus infection. Trichostrongylus deflexus has been described as a separate species only relatively recently (Boomker & Reinecke 1989). Echinococcus Mönnig (1933) described specimens of Trichostrongylus Hydatid cysts were recovered from the lungs of one warthog. instabilis from impala with extreme variation in the spicule Echinococcus granulosus has remarkably low intermediate shape. Similarly, Horak (1980) found the same extreme host specificity (MacPherson 1985). Hydatid cysts have been variation in spicule shape from Trichostrongylus males that recovered from many species, including impalas, warthogs he recovered from sheep, calves and goats that had been and zebras (Equus burchellii) (Young 1975). Possible definitive artificially infected from faecal cultures of impalas. He hosts of Echinococcus spp. on the farm in Lephalale are referred to these worms as Trichostrongylus colubriformis. spotted hyenas (Crocuta crocuta), black-backed jackals (Canis Boomker and Reinecke (1989) re-evaluated some of these mesomelas), African wild cat (Felis lybica) (Verster & Collins specimens and proposed that these worms represent a 1966), and domestic dogs. definitive species, which they named T. deflexus. Horak et al. (1983b) reported T. colubriformis from blue wildebeest from Taenia spp. the Kruger National Park. They made no mention of the The larval stage of T. hydatigena is much larger than that spicule morphology. After examining the material collected of other species and is thus more easily identified (Verster et al by Horak . (1983b) from the wildebeest, Boomker and 1969). The intermediate hosts are ruminants and pigs, whilst T. colubriformis Reinecke (1989) considered from this material the final hosts are canines and other wild carnivores. In sheep as synonymous with T. deflexus. Trichostrongylus deflexus was the migratory tracts through the liver, commonly known recovered from blue wildebeest and impalas in the current as hepatitis cysticercosa, can cause the death of an animal study. (Reinecke 1983). No macroscopic liver pathology was noted in any of the gemsbok affected. Trichuris Ortlepp (1937) described Trichuris barbertonensis from an ox. Taenia hyaenae utilises many ruminant species as intermediate The spicules and sheath measured between 6.83 mm and hosts. The definitive hosts for this species are hyaenas and 7.3 mm and did not end in a bulb or swelling as is described African wild dogs (Lycaon pictus) (Loos-Frank 2000). Spotted for Trichuris globulosa or Trichuris ovis. Two individual adult hyaenas, brown hyaenas (Hyaena brunnea), African wild Trichuris worms were recovered from the large intestine of dogs, black-backed jackals and leopards (Panthera pardus) are

http://www.ojvr.org doi:10.4102/ojvr.v78i1.308 Page 9 of 11 Original Research all known to frequent the farm from which these gemsbok Conclusion came. Cysticerci that resemble this species in the number and shape of the rostellar hooks have previously been recovered The aim of the study was to describe the helminth parasites from impalas and sable antelopes (Hippotragus niger) (Verster of the common wildlife species in the northern and western 1969). Macroscopically it cannot be distinguished from the parts of the Limpopo province. The climate of these areas cysticerci of other Taenia spp., including Taenia saginata. Only is harsh and dry, with a large region that is considered to be semi-arid. This has an impact on the prevalence of the microscopically can T. saginata be identified by the absence parasites that occur in these areas. In total 36 animals were of rostellar hooks, an important consideration during meat examined and their helminths recorded. New host records inspection. Humans are the definitive hosts for the latter for species include A. gorgonis in black wildebeest, S. cestode, which has been recovered from various game globipunctata in waterbuck and F. hepatica in kudu. species. Larval T. saginata has been found in several hosts in Africa; for example Graber (1959) found the species in For the study area as a whole, comparisons with other Dorcas gazelles (Gazella dorcas), red-fronted gazelles (Gazella studies provided valuable information. The total burdens rufifrons) and Gazella spp. in Chad, Le Roux (1937) observed it and species variation of especially the adult helminths in in oribis (Ourebia ourebi) in Zambia, Sousa Dias (1950) found this study were consistently lower compared with studies in it in Cape buffaloes (Syncerus caffer) in Angola and Nelson, areas with higher rainfall. Pester and Rickman (1965) in bushbuck in Kenya. Also, the metacestodes of Taenia solium have been found in warthogs The only trematode recovered was F. hepatica from a kudu in Africa (Bain 2001) and in wild boars (Sus scrofa) in Europe at Nwanedi. The dry climate is not conducive to the survival (Eslami & Farsad-Hamdi 1992). It is evident that there is a of freshwater snails that act as intermediate hosts. These potential public health risk associated with the consumption parasites typically occur in areas with wetter or more humid of venison infected with metacestodes. conditions.

Hydatid material of human origin collected in sub-Saharan There are practical implications for the low prevalence Africa all conform to the sheep strain of E. granulosus and species variation of helminths. When animals are (MacPherson & Wachira 1997). However, this does not translocated from the drier parts of the Limpopo province to prove non-infectivity of other E. granulosus strains, species areas with higher rainfall, they will be relatively naive to the or subspecies to humans. Because of the seriousness of higher parasite loads in those areas and/or completely naive Echinococcus spp. infection, meat inspection should be to other parasites, such as lungworms. On the other hand, thorough and the necessary precautions should be taken animals originating from areas with higher rainfall are likely when handling carnivores (Young 1975). to harbour higher parasite loads. They should be dewormed prior to translocation to dry areas, because the stress of the Fasciola dry climate and change in vegetation can cause them to succumb to the parasite loads they already harbour. At the Two specimens of F. hepatica were recovered from a kudu same time, new parasites could be introduced, with variable from the Nwanedi Game Reserve. Fasciola hepatica has not results to the wildlife already present. been described from kudus previously. As browsers, kudus are not normally exposed to aquatic vegetation and thus few Game is kept together with domestic stock on many get infected with trematodes (Condy 1972). Fasciola gigantica farms in the province. Helminths that typically occur in has been reported in Greater kudu on a game ranch in Zambia domestic stock were recovered from some antelope species. (Zieger et al. 1998) as well as in Rhodesia (now Zimbabwe), Haemonchus contortus was recovered from all the kudus and where kudu deaths were attributed to this parasite (Condy blue wildebeest from Langgedachte. High stocking densities 1972; Hammond 1972). Kudus appear to be very susceptible of animals on this farm likely contributed to the frequency to infection (Condy 1972). of cross-transmission of parasites between species. With parasites that have a high fecundity, such as Haemonchus The Nwanedi Nature Reserve, where the infected kudu was or Oesophagostomum, environmental build-up may become examined, has a large dam that is fed by the Nwanedzi river. considerable under certain conditions or specific times of This creates a favourable environment for the freshwater snail the year. This will impact on worm control programmes for that serves as intermediate host to the flukes. Domestic stock domestic animals, but may also cause morbidity in game at have previously had access to the reserve and are currently times. kept upstream from the dam, which could be a possible source of contamination. Wildlife that have been introduced Some parasites are more problematic in intensive situations, to the reserve are other possible sources. Fasciola gigantica is for example when animals are kept in a boma or very small the most common liver fluke in domestic ruminants in Africa camps. This is especially true for parasites with a monoxenous and accounts for most liver fluke infections in wild animals life cycle such as Trichuris spp. Animals that are kept (Hammond 1972). intensively should be dewormed to prevent environmental

http://www.ojvr.org doi:10.4102/ojvr.v78i1.308 Page 10 of 11 Original Research build-up of the parasite. Under extensive conditions, these References parasites are unlikely to cause any problems. Acocks, J.P.H., 1988, Veld types of South Africa. Botanical Research Institute, Pretoria. (Memoirs of the Botanical Survey of South Africa, no. 57) The only known zoonotic helminth recovered was E. Anderson, I.G., 1992, ‘Observations on the life-cycles and larval morphogenesis of, and transmission experiments with Cooperioides hamiltoni and Cooperioides granulosus from the lungs of a warthog. The infective stage for hepaticae (Nematoda: Trichostrongyloidea) parasites in impala, Aepyceros humans is the egg that is deposited by the final host – dogs melampus’, South African Journal of Zoology 27, 81–87. Bain, R.K., 2001, ‘Africa’, in N. Chowdury & A.A. Aguierra (eds.), Helminths of wildlife, – which are often fed uncooked offal. One should be aware pp. 371–424, Science Publications, Enfield. that the parasite can become established in the local human Boomker, J., 1977, ‘A revision of the genus Impalaia Mönnig, 1924’, Onderstepoort population through this route, especially in communal areas Journal of Veterinary Research 44, 131–138. PMid:614530 Boomker, J., Keep, M.E., Flamand, J.R. & Horak, I.G., 1984, ‘The helminths of various where people live in close association with their animals. antelope species from Natal’, Onderstepoort Journal of Veterinary Research 51, 253–256. Boomker, J., Horak, I.G. & De Vos, V., 1986, ‘The helminth parasites of various Cysticerci of T. hyaenae and T. hydatigena were recovered artiodactylids from some South African nature reserves’, Onderstepoort Journal of Veterinary Research 53, 93–102. PMid:3725333 from the gemsbok. Although these tapeworms are not Boomker, J., Anthonissen, M. & Horak, I.G., 1988, ‘Parasites of South African wildlife. known to be zoonotic, the cysticerci are not macroscopically II. Helminths of kudu, Tragelaphus strepsiceros, from South West Africa/Namibia’, Onderstepoort Journal of Veterinary Research 55, 231–233. PMid:3217096 distinguishable from the zoonotic cysticeri of T. solium or Boomker, J., Horak, I.G. & De Vos, V., 1989, ‘Parasites of South African wildlife. IV. T. saginata. This has public health implications because the Helminths of kudu, Tragelaphus strepsiceros, in the Kruger National Park’, Onderstepoort Journal of Veterinary Research 56, 111–121. PMid:2748130 cysticerci render the meat aesthetically unacceptable and, in Boomker, J. & Reinecke, R.K., 1989, ‘Trichostrongylus deflexus n. sp. (Nematoda: addition, a lack of proof of non-infectivity does not prove Trichostrongylidae) from several antelope species’, South African Journal of Wildlife Management 19, 21–25. that these cestodes are not in fact infective to humans. Boomker, J., Horak, I.G., Booyse, D.G. & Meyer, S., 1991a, ‘Parasites of South African wildlife. VIII. Helminth and arthropod parasites of warthogs, Phacochoerus aethiopicus, in the Eastern Transvaal’, Onderstepoort Journal of Veterinary The host species included in the study are some of the Research 58, 195–202. PMid:1923382 more common ones that occur on game farms in the Boomker, J., Horak, I.G. & Knight, M.M., 1991b, ‘Parasites of South African wildlife. IX. Helminths of kudu, Tragelaphus strepsiceros, in the Eastern Cape Province‘, Limpopo province. The parasites of many wildlife species, Onderstepoort Journal of Veterinary Research 58, 203–204. PMid:1923383 including relatively common species such as giraffes (Giraffa Boomker, J., Horak, I.G., Watermeyer, R. & Booyse, D.G., 2000, ‘Parasites of South African wildlife. XVI. Helminths of some antelope species from the Eastern and camelopardalis), common reedbuck (Redunca arundinum) Western Cape Provinces’, Onderstepoort Journal of Veterinary Research 67, 31– 41. PMid:10843320 (Boomker et al. 1984) and grey rhebuck (Pelea capreolus) (see Boomker, J., 2007, Helminth infections: Wildlife. University of Pretoria, Pretoria. Boomker et al. 2000) but also scarcer game such as red duikers Condy, J.B., 1972, ‘Observations on levels of internal parasites in free living Rhodesian (Cephalophus natalensis) (see Boomker et al. 1984), have wild life. I. Kudu (Tragelaphus strepsiceros [Pallas, 1926])’, Zoologica Africana 7, 413–418. not been studied extensively, particularly in the Limpopo Eslami, A. & Farsad-Hamdi, S., 1992, ‘Helminth parasites of wild boar, Sus scrofa, in province. Because these animals all share the same, mostly Iran’, Journal of Wildlife Diseases 28, 316–315. PMid:1602589 Gallivan, G.J., Barker, I.K., Alves, R.M.R., Culverwell, J. & Girdwood, R., 1989, confined environment, scientific game farming practices ‘Observations on the lungworm, Pneumostrongylus calcaratus, in impala require more knowledge on the parasites, including the (Aepyceros melampus) from Swaziland’, Journal of Wildlife Diseases 25, 76–82. PMid:2915405 helminths, of these species. Gallivan, G.J., Barker, I.K., Culverwell, J. & Girdwood, R., 1996, ‘Prevalence of hepatic helminths and associated pathology in impala (Aepyceros melampus) in Swaziland’, Journal of Wildlife Diseases 32, 137–141. PMid:8627927 Gibbons, L.M., Jones, A. & Khalil, L.F., 1996, Eighth international training course Acknowledgements on identification of helminth parasites of economic importance, International The project was funded partly by a study bursary from Institute of Parasitology, St. Albans. Graber, M., 1959, La cysticercose bovine. Son importance dans les zones sahéliennes the Department of Agriculture, Limpopo. The late Mr. d’elevage de la Republique du Tschad. [Bovine cysticercosis. Its importance in the Sahelian areas of livestock of the Republic of Chad]. Revue Ềlevage de Médicine Ryno Watermeyer from the Helminthology section at the vétérinaire Pays tropicale 12, 121–143. Department of Veterinary Tropical Diseases and Ms. I. Hammond, J.A., 1972, ‘Infections with Fasciola spp. in wildlife in Africa’, Tropical Venter of the Louis Trichardt State Veterinary Laboratory are Animal Health 4, 1–13. http://dx.doi.org/10.1007/BF02357089, PMid:4671397 Heinichen, I.G., 1973, ‘Parasitological studies on impala: preliminary report’, Journal thanked for their technical assistance. Thanks also go to Mr. of the South African Veterinary Association 44, 265–269. PMid:4787763 R. van Wyk of the Musina Research Station, Mr. S. Joubert of Horak, I.G., 1978, ‘Parasites of domestic and wild animals in South Africa. X. Helminths of impala’, Onderstepoort Journal of Veterinary Research 45, 221–228. Kerneels Young Trust, Mr. M. Vermaas of Langgedachte, Mr. PMid:572950 N. van Zyl of Bushman’s Safaris and Mr. C. van Heerden, for Horak, I.G., 1980, ‘The incidence of helminths in pigs, sheep, cattle, impala and blesbok in the Transvaal’, PhD thesis, Dept. of Zoology and Entomology, University making material available. of Natal. Horak, I.G., 1981, ‘Host specificity and the distribution of the helminth parasites in sheep, cattle, impala and blesbok according to climate’, Journal of the South Competing interests African Veterinary Association 52, 201–206. PMid:7310791 Horak, I.G., Biggs, H.C., Hanssen, T.S. & Hanssen, R.E., 1983a, ‘The prevalence of The authors declare that there were no competing interests helminth and arthropod parasites of warthog, Phacochoerus aethiopicus, in South West Africa/Namibia’, Onderstepoort Journal of Veterinary Research 50, 145–148. that may have inappropriately influenced the presentation of PMid:6634088 information in this paper. Horak, I.G., De Vos, V. & Brown, M.R., 1983b, ‘Parasites of domestic and wild animals in South Africa. XVI. Helminth and arthropod parasites of blue and black wildebeest (Connochaetes taurinus and Connochaetes gnou)’, Onderstepoort Journal of Veterinary Research 50, 243–255. PMid:6676686 Authors’ contributions Horak, I.G., Boomker, J., De Vos, V. & Potgieter, F.T., 1988, ‘Parasites of domestic and wild animals in South Africa. XXIII. Helminth and arthropod parasites of warthogs, I.C.v.W. conducted the study in partial fulfillment of an Phacochoerus aethiopicus, in the Eastern Transvaal Lowveld’, Onderstepoort Journal of Veterinary Research 55, 145–152. PMid:3194114 MSc degree. J.B. acted as supervisor for the thesis and made Le Roux, P.L., 1937, Annual report of the Veterinary Department, Northern Rhodesia conceptual and editorial contributions. 1936, Appendix C, pp. 62–63, Government Printer, Livingstone.

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Loos-Frank, B., 2000, ‘An up-date of Verster’s (1969) ‘Taxonomic revision of the genus Reinecke, R.K., 1983, Veterinary helminthology, Butterworth, Pretoria. Taenia Linnaeus’ (Cestoda) in table format’, Systematic Parasitology 45, 155–183. http://dx.doi.org/10.1023/A:1006219625792, PMid:10768761 Round, M.C., 1968, ‘Check list of the helminth parasites of African mammals of the orders Carnivora, Tubulidentata, Proboscidea, Hyracoidea, Artiodactyla and MacPherson, C.N.L., 1985, ‘Echinococcus infections in wild animals in Africa’, in S. Perissodactyla’, Technical Communication of the Commonwealth Bureau of MacMillan (ed.), Proceedings of a conference on wildlife/livestock interfaces on Helminthology 38, pp. vi and 252. rangelands, Taita Hills, Kenya, April 22–25, 1985, pp. 73–78. Sousa Dias, V.A., 1950, Nota prévia sôbre os parasitas dos animais domésticos de MacPherson, C.N.L. & Wachira, T.W.M., 1997, ‘Cystic echinococcosis in Africa south of the Sahara’, in F.L. Andersen, H. Ouhelli & M. Kachani (eds.), Compendium Angola. [Notes on the prevalence of parasites of domestic animals in Angola]. on cystic echinococcosis in Africa and in Middle Eastern countries with special Pecuária: anais dos Serviços de Veterinária e Indústria Animal da Colónia de reference to Morocco, pp. 245–277, Brigham Young University, Provo. Angola 2, 53–59. Mönnig, H.O., 1933, ‘Wild antelopes as carriers of nematode parasites of domestic South African Weather Service, 2007, Rainfall (mm) for the season July 2006 to June ruminants – Part III’, Onderstepoort Journal of Veterinary Science and Animal 2007, viewed 10 October 2007, from http://www.weathersa.co.za/RainfallMaps/. Industry 1, 77–92. Verster, A. & Collins, M., 1966, ‘The incidence of hydatidosis in the Republic of South Nelson, G.S., Pester, F.R.N. & Rickman, R., 1965, ‘The significance of wild animals in Africa’, Onderstepoort Journal of Veterinary Research 33, 49–72. PMid:6007781 the transmission of cestodes of medical importance in Kenya’, Transactions of the Royal Society of Tropical Medicine and Hygiene 57, 507–524. http://dx.doi. Verster, A., 1969, ‘A taxonomic revision of the genus Taenia Linnaeus, 1758’, org/10.1016/0035-9203(65)90153-7 Onderstepoort Journal of Veterinary Research 36, 3–58. PMid:5407584 Ortlepp, R.J., 1937, ‘Whipworms from South African ruminants’, Onderstepoort Young, E., 1975, ‘Echinococcosis (hydatidosis) in wild animals of the Kruger Journal of Veterinary Science and Animal Industry 9, 91–100. National Park’, Journal of the South African Veterinary Association 46, 285–286. PMid:1219111 Ortlepp, R.J., 1962, ‘Lungworms from South African antelopes’, Onderstepoort Journal of Veterinary Research 29, 173–181. Young, E. & Wagener, L.J.J., 1968, ‘The impala as a source of food and by-products. Ortlepp, R.J., 1964, ‘Observations on helminths parasitic in warthogs and bushpigs’, Data on production potential, parasites and pathology of free-living impalas in the Onderstepoort Journal of Veterinary Research 31, 11–38. Kruger National Park’,Journal of the South African Veterinary Medical Association 39, 81–86. Pletcher, J.M., Horak, I.G., De Vos, V. & Boomker, J., 1988, ‘Hepatic lesions associated with Cooperioides hepaticae (Nematoda: Trichostrongyloidea) infection in impala Zieger, U., Boomker, J., Cauldwell, A.E. & Horak, I.G., 1998, ‘Helminths and botfly larvae (Aepyceros melampus) of the Kruger National Park’, Journal of Wildlife Diseases of wild ungulates on a game ranch in Central Province, Zambia’, Onderstepoort 24, 650–655. PMid:3193559 Journal of Veterinary Research 65, 137–141. PMid:9741058

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